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Myrionema strangulans (Chordariales, Phaeophyceae) epiphyte on Ulva spp. (Ulvophyceae) from Patagonian Atlantic coasts

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Abstract

Fronds of Ulva spp. from Patagonian Atlantic coasts exhibited brown spots produced by the presence of Myrionema strangulans (Chordariales, Phaeophyceae). The occurrence of M. strangulans on Ulva spp. is widely reported from several regions of the world, but there were no detailed studies about the subject. In the present study, we describe the morphology and interactions of M. strangulans with Ulva spp. as observed under light and electron microscopes, and we reconstruct all stages of its life cycle based upon in vitro experiments. The prevalence of infection by M. strangulans was 100%. In case of the strongest epiphytism, the host cuticle exhibited perforations, massive depigmentation, cellular disorganization, and cuticle rupture. It was possible to demonstrate a purely epiphytic life strategy of the organism by transmission electron microscopy. M. strangulans formed discoid thalli constituted by vegetative filaments and radiating from a central zone to a peripheral zone. Transversally, the discs were formed by two strata: a basal monostromatic and a filamentous erect stratum. From the monostromatic stratum, hyaline hairs and reproductive structures were produced. Both plurilocular and unilocular sporangia were present. Zoids from both plurilocular and unilocular sporangia were able to germinate in culture. M. strangulans exhibited a haploid–diploid, heteromorphic life cycle with thalli with three different morphologies. The haploid chromosome number was 12 ± 2 chromosomes.

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References

  • Adami ML, Gordillo S (1999) Structure and dynamics of the biota associated with Macrocystis pyrifera (Phaeophyta) from the beagle channel, Tierra del Fuego. Sci Mar 63:183–191

    Article  Google Scholar 

  • Anderson RJ, Levitt GJ. Dawes CP, Simons RH (1992) Experimental growth of Gracilaria in Saldanha Bay. South Africa. In: Mshigeni KE, Bolton J. Critchley A, Kiangi G (eds), Proceedings of the First International Workshop on Sustainable Seaweed Resource Development in Sub-Saharan Africa. KE Mshigeni, Windhoek, Namibia:19–36

  • Asensi A (1966) Guía para reconocer los géneros de algas pardas de la Argentina. Contr Inst Antart Arg 103:1–51

    Google Scholar 

  • Bastida R (1968) Preliminary notes of the marine fouling at the port of Mar del Plata (Argentina). C R II Int Cong Mar Foul Corros 557–562

  • Bolton JJ, Robertson-Andersson DV, Shuuluka D, Kandjengo L (2009) Growing Ulva (Chlorophyta) in integrated systems as a commercial crop for abalone feed in South Africa: a SWOT analysis. J Appl Phycol 21:575–583

    Article  Google Scholar 

  • Boraso de Zaixo AL (1977) El género Ulva (Algae, Chlorophyta) I. Ulva en Puerto Deseado (Provincia de Santa Cruz). Darwiniana 21(1):162–171

    Google Scholar 

  • Boraso de Zaixo AL, Rico AE, Perales S, Pérez L, Zalazar H (2004) Algas Marinas de la Patagonia Una guía ilustrada, Universidad Nacional de la Patagonia San Juan Bosco–CONICET. Chubut, Argentina

    Google Scholar 

  • Buschmann AH, Gómez P (1993) Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes. Hydrobiologia 260/261:345–351

    Article  Google Scholar 

  • Buschmann AH, Kuschel FA (1988) Cultivo intermareal de Gracilaria sp. colonización de esporas e interacción con Ulva lactuca. Biota 4:107–113

    Google Scholar 

  • Buschmann AH, Kuschel FA, Perez E (1990) Field assessment of intertidal culture of Gracilaria (Rhodophyta: Gigartinales) in southern Chile. In: Oliveira E, Kautsky N (eds) Cultivation of seaweeds in latin America. Universidad de Sao Paulo/IFS, Brazil, pp 69–74

    Google Scholar 

  • Caram B (1961) Sur l’alternance de générations et de phase cytologiques chez le Sauvageaugloia griffithsiana (Greville) Hamel. C R Séanc Acad Sci 252:594–596

    Google Scholar 

  • Caram B (1965) Recherches sur la reproduction et le cycle sexué de quelques Phéophycées. Vie et Milieu 16:21–222

    Google Scholar 

  • Christensen T (1982) Alger i naturen og i laboratoriet. Nucleus Århus, Denmark

    Google Scholar 

  • Cohen I, Neori A (1991) Ulva lactuca biofilters for marine fishpond effluents. 1. Ammonia uptake kinetics and nitrogen content. Bot Mar 34:475–482

    Article  Google Scholar 

  • Cole K (1967) Chromosome numbers in the Phaeophyceae. Can J Genet Cytol 9:519–530

    Google Scholar 

  • Colorni A (1989) Perforation disease affecting Ulva sp. cultured in Israel on the Red Sea. Disease Aquat Organ 7:71–73

    Article  Google Scholar 

  • De Busk TA, Blakeslee M, Ryther JH (1986) Studies on outdoor cultivation of Ulva lactuca L. Bot Mar 29:381–386

    Article  Google Scholar 

  • Draisma SGA, Prud’homme van Reine WF, Stam WT, Olsen JA (2001) A reassessment of phylogenetic relationships within the phaeophyceae based on RUBISCO large subunit and ribosomal DNA sequences. J Phycol 37:586–603

    Article  Google Scholar 

  • Fletcher RL (1987) Seaweeds of the British Isles. Fucophyceae (Phaeophyceae), vol 3. British Museum (Natural History), London

    Google Scholar 

  • Friedlander M (1992) Gracilaria conferta and its epiphytes: the effect of culture conditions on growth. Bot Mar 35:423–428

    Article  Google Scholar 

  • Friedlander M, Shalev R, Ganor T, Strimling S, Ben-Amotz A, Klar H, Wax Y (1987) Seasonal fluctuations of growth rate and chemical composition of Gracilaria cf. conferra in outdoor culture in Israel. Hydrobiologia 151/152:501–507

    Article  Google Scholar 

  • Friedlander M, Krom MD, Ben Amotz A (1991) The effect of light and ammonium on growth, epiphytes and chemical constituents of Gracilaria conferta in outdoor cultures. Bot Mar 34:161–166

    Article  CAS  Google Scholar 

  • Fritsch FE (1945) The structure and reproduction of the algae. Foreword, Phaeophyceae, Rhodophyceae, Myxophyceae, vol 2. University Press, Cambridge

    Google Scholar 

  • Gauna MC (2010) Bioecología y relaciones interespecíficas en poblaciones de dos algas pardas del Atlántico Occidental Sur y Norte: Dictyota dichotoma y Ascophyllum nodosum, PhD thesis, Universidad Nacional del Sur, Argentina

  • Gauna MC, Parodi ER (2008) Green epi-endophytes in Hymenena falklandica (Rhodophyta) from the patagonian coasts of Argentina: preliminary observations. Phycol Res 56:172–182

    Article  Google Scholar 

  • Gauna MC, Parodi ER, Cáceres EJ (2007) Epi-endophytic symbiosis between Laminariocolax aecidioides (Ectocarpales, Phaeophyceae) and Undaria pinnatífida (Laminariales, Phaeophyceae) growing on Argentinean coasts. J Appl Phycol 21:11–18

    Article  Google Scholar 

  • Gauna MC, Parodi ER, Cáceres EJ (2009) Epiphytic relationships of Pseudendoclonium submarinum Wille (Ulvophyceae) and Rhodymenia pseudopalmata (Rhodophyta) from the Patagonian coast of Argentina. Phycol Res 57:313–322

    Article  Google Scholar 

  • Greville RK (1827) Some account of a collection of cryptogamic plants from the Ionian Islands. Trans Linn Soc London 15:335–348

    Article  Google Scholar 

  • Guiry MD (1978) An appraisal of the Irish benthic marine algal flora. Brit Phycol J 13:1–200

    Article  Google Scholar 

  • Haglund K (1992) Photosynthesis and growth of some marine algae, with emphasis on the rhodophyte Gracilaria tenuistipitata. Acta Univ Ups, Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science 377. Uppsala, Sweden, 48 pp

  • Hayden HS, Blomster J, Maggs CA, Silva PC, Stanhope MJ, Waaland JR (2003) Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur J Phycol 38:277–294

    Article  Google Scholar 

  • Irvine DEG (1982) Seaweeds of the Faroes 1: The flora. B Brit Mus (Natural History) Bot 10:109–131

    Google Scholar 

  • Israel A, Friedlander M, Neori A (1993) Biomass, yield, photosynthesis and morphological expression of Ulva lactuca. Bot Mar 38:297–302

    Article  Google Scholar 

  • Jiménez del Río M, García Reina G, Ramazanov Z (1996) Ulva rigida (Ulvales, Chlorophyta) tank culture as biofilters for dissolved inorganic nitrogen from fishpond effluents. Hydrobiologia 326/327:61–66

    Article  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw Hill, New York

    Google Scholar 

  • Kawai H (1986) Life history and systematic position of Akkesiphycus lubricus (Phaeophyceae). J Phycol 22:286–291

    Article  Google Scholar 

  • Kornmann P, Sahling PH (1983) Meeresalgen von Helgoland: Ergänzung. Biologische Anstalt Helgoland, Hamburg, pp 46–50

    Google Scholar 

  • Kühnemann O (1972) Bosquejo fitogeográfico de la vegetación marina del litoral argentino. Physis 31(82):117–142, 31(83):295–325

    Google Scholar 

  • Kuschel FA, Buschmann AH (1991) Abundance effects and management of epiphytism in intertidal cultures of Gracilaria (Rhodophyta) in southern Chile. Aquaculture 92:7–19

    Article  Google Scholar 

  • Lee RKS (1980) A catalogue of the marine algae of the Canadian Arctic. Nat Mus Can Publ Bot 9:1–82

    Google Scholar 

  • Lewin J (1966) Silicon metabolism in Diatoms 5: Germanium dioxide, a specific inhibitor of diatom growth. Phycologia 6:1–12

    Article  CAS  Google Scholar 

  • Lindauer VW, Chapman VJ, Aiken M (1961) The marine algae of New Zealand. II. Phaeophyceae. Nova Hedwigia 3:129–350

    Google Scholar 

  • Loiseaux S (1964a) Sur une nouvelle espèce de Myrionema des environs de Roscoff et son cycle. Cr Herb Acad Sci 259:383–2385

    Google Scholar 

  • Loiseaux (1964b) Sur’hétéroblastie et le cycle de deux Ascocyclus de la región de Roscoff. Cr Herb Acad Sci 259:2903–2905

    Google Scholar 

  • Loiseaux S (1967a) Morphologie et cytologie des Myrionémacées. Critères taxonomiques. Rev Gen Bot 74:329–350

    Google Scholar 

  • Loiseaux S (1967b) Recherches sur les cycles de développement des Myrionématées (Phéophycées) I–II Hécatonématées et Myrionématées. Rev Gen Bot 74:1–529

    Google Scholar 

  • Loiseaux S (1968) Sur les phénomènes d’hétéroblastie et de dimorphisme chez les Phéophycées. Rev Gen Bot 75:229–244

    Google Scholar 

  • Loiseaux S (1970) Notes on several Myrionemataceae from California using culture studies. J Phycol 6:248–260

    Google Scholar 

  • Loiseaux S (1972) Variations des cycles chez les Myrionématacées et leur signification phylogénétique. Soc Bot Fr Mémoires 105–116

    Google Scholar 

  • Loiseaux de Goër S, Noailles MC (2008) Algues de Roscoff. Roscoff: Editions de la Station Biologique de Roscoff

    Google Scholar 

  • López Rodríguez MC, Pérez-Cirera JL (1995) Fragmenta Chorologica Occidentalia, Algae 5157–5166. An Jar Bot Madrid 52:197–198

    Google Scholar 

  • Martín LA, Boraso de Zaixso AL, Leonardi PI (2011) Biomass variation and reproductive phenology of Gracilaria gracilis in a Patagonian natural bed (Chubut, Argentina). J Appl Phycol 23:643–654

    Google Scholar 

  • Miravalles AB (2009) Biología y ultraestructura de Codium spp. (Bryopsidophyceae, Chlorophyta): morfologías vegetativa y reproductiva, ciclos de vida y epifitismo. PhD thesis, Universidad Nacional del Sur, Argentina

    Google Scholar 

  • Mol I, Coppejans E (1985) Algues marines nouvelles pour la côte du Boulonnais (Pas-de-Calais, France). II. B Soc Roy Bot Belg 118:233–243

    Google Scholar 

  • Morton O (2003) The marine macroalgae of County Donegal, Ireland. B Irish Biogeog Soc 27:3–164

    Google Scholar 

  • Neori A, Shpigel M (1999) Algae treat effluents and feed invertebrates in sustainable integrated mariculture. World Aquac 30:46–49

    Article  Google Scholar 

  • Neori A, Cohen I, Gordin H (1991) Ulva lactuca biofilter for marine fish pond effluents. 2. Growth rate, yield and C/N ratio. Bot Mar 34:483–489

    Article  Google Scholar 

  • Neori A, Krom MD, Boyd CE, Popper D, Rabinovitch R, Davison PJ, Dvir O, Zuber D, Ucko M, Angel D, Gordin H (1996) Seaweed biofilters as regulators of water quality in integrated fish-seaweed culture units. Aquaculture 141:183–199

    Article  Google Scholar 

  • Neori A, Ragg NLC, Shpigel M (1998) The integrated culture of seaweed abalone, fish and clams in modular intensive land-based systems. II. Performance and nitrogen partitioning within an abalone (Haliotis tuberculata) and macroalgae culture system. Aquacult Eng 17:215–239

    Article  Google Scholar 

  • Neori A, Shpigel M, Ben-Ezra D (2000) A sustainable integrated system for culture of fish, seaweed and abalone. Aquaculture 186:279–291

    Article  Google Scholar 

  • Neori A, Msuya F, Shauli L, Schuenhoff A, Kopel F, Shpigel M (2003) A novel three-stage seaweed (Ulva lactuca) biofilter design for integrated mariculture. J Appl Phycol 15:543–553

    Article  CAS  Google Scholar 

  • Norton TA (1970) The marine algae of county Wexford, Ireland. Brit Phycol J 5:257–266

    Article  Google Scholar 

  • Núñez O (1968) An acetic-haematoxylin squash method for small chromosome. Caryologia 21:115–119

    Google Scholar 

  • O’Kelly CJ, Kurihara A, Shipley TC, Sherwood AR (2010) Molecular assessment of Ulva spp. (Ulvophyceae, Chlorophyta) in the Hawaiian islands. J Phycol 46:728–735

    Article  Google Scholar 

  • Ohno M (1993) Cultivation of the green algae, Monostroma and Enteromorpha “Anori”. In: Ohno M, Critchley AT (eds) Seaweed cultivation and marine ranching. Japan International Cooperation Agency, Yokusuka, pp 7–15

    Google Scholar 

  • Papenfuss GF (1964) M.O. Parthasarathy Iyengar. Phytomorphology 14:328–330

    Google Scholar 

  • Parker BC (1981) Phycologia Triginta Quinque. J Phycol 17:360–371

    Article  Google Scholar 

  • Peters AF, Schaffelke B (1996) Streblonema (Ectocarpales, Phaeophyceae) infection in the kelp Laminaria saccharina (Laminariales, Phaeophyceae) in the western Baltic. Hydrobiologia 326/327:111–116

    Article  Google Scholar 

  • Pickering TD, Gordon ME, Tong LJ (1993) Effect of nutrient pulse concentration and frequency on growth of Gracilaria chilensis plants and levels of epiphytic algae. J Appl Phycol 5:525–533

    Article  Google Scholar 

  • Piriz ML (1972) Los organismos incrustantes de las Costas Argentinas. II. Estudio preliminar de la ficoflora y fauna asociada a Ulva lactuca L. (Algae, Chlorophyta) en el Puerto de Mar del Plata. (Argentina). An Lab Ens Mat Inv Tecn Prov Bs As Ser II 219:5–98

    Google Scholar 

  • Provasoli L (1968) Media and prospect for the cultivation of marine algae. In: Watanabe A (ed) Cultures and collections of algae. Japanese Society for Plant Physiology, Japan, pp 1–63

    Google Scholar 

  • Ramirez ME, Santelices B (1991) Catálogo de las algas marinas bentónicas de la costa temperada del Pacífico Sudamericano. Monograf Biol 5:1–499

    Google Scholar 

  • Reymond O, Pickett-Heaps JD (1983) A routine flat embedding method for electron microscopy of microorganisms allowing selection and precisely oriented sectioning of single cells by light microscopy. J Microsc 130:79–84

    Article  PubMed  CAS  Google Scholar 

  • Rico A, Pérez L, Perales S (1993) Especies del género Enteromorpha (Chlorophyta) en los alrededores de Comodoro Rivadavia, Chubut (Argentina). Nat Patagón Ser Cienc Biol 1:103–107

    Google Scholar 

  • Robertson-Andersson DV (2003) The cultivation of Ulva lactuca (Chlorophyta) in an integrated aquaculture system, for the production of abalone feed and the bioremediation of aquaculture effluent. MSc thesis, University of Cape Town, South Africa

    Google Scholar 

  • Robertson-Andersson DV (2007) Biological and economical feasibility studies of using seaweeds Ulva lactuca (Chlorophyta) in recirculation systems in abalone farming. PhD thesis, University of Cape Town, South Africa

    Google Scholar 

  • Robertson-Andersson DV, Potgieter M, Hansen J, Bolton JJ, Troell M, Anderson RJ, Halling C, Probyn T (2008) Integrated seaweed cultivation on an abalone farm in South Africa. J Appl Phycol 20:570–595

    Article  Google Scholar 

  • Schneider CW, Searles RB (1991) Seaweeds of the southeastern United States, Cape Hatteras to Cape Canaveral, Durham and London. Duke University Press, Durham

    Google Scholar 

  • Schuenhoff A, Shpigel M, Lupatsch I, Ashkenazi A, Msuya FE, Neori A (2003) A semirecirculating, integrated system for the culture of fish and seaweed. Aquaculture 221:167–181

    Article  Google Scholar 

  • Siemer BL, Stam WT, Olsen JL, Pedersen PM (1998) Phylogenetic relationships of the brown algal orders Ectocarpales, Chordariales, Dictyosiphonales, and Tilopteridales (Phaeophyceae) based on Rubisco large subunit and spacer sequences. J Phycol 34:1038–1048

    Article  CAS  Google Scholar 

  • Silva PC, Chacana ME (2005) Marine algae from Islas San Félix y San Ambrosio (Chilean Oceanic Islands). Cryptogamie Algol 26:103–118

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  PubMed  CAS  Google Scholar 

  • Taylor WR (1957) Marine algae of the northeastern coast of North America. University of Michigan Press, Michigan

    Google Scholar 

  • Ugarte R, Santelices B (1992) Experimental tank cultivation of Gracilaria chilensis in central Chile. Aquaculture 101:7–16

    Article  Google Scholar 

  • Womersley HBS (1987) The marine benthic flora of southern Australia. Part II. Adelaide. South Australian Government Printing Division, Australia

    Google Scholar 

  • Wynne MJ, Loiseaux S (1976) Phycological reviews 5: recent advances in life history studies of the phaeophyta. Phycologia 15:435–452

    Article  Google Scholar 

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Acknowledgments

MCG is a post-doctoral research fellow from the National Council of Scientific and Technical Research of Argentina (CONICET) and ERP is a researcher of CONICET. EJC is a researcher of the Commission of Scientific Research of the Province of Buenos Aires, Argentina (CIC). Support was provided by grants from the Secretaría de Ciencia y Tecnología de la Universidad Nacional del Sur (PGI CSU-24/B145) and CONICET (PIP-11220100100503). We are also grateful to Bch. Croce, María Emilia for her participation in the first instances of this work.

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Siniscalchi, A.G., Gauna, M.C., Cáceres, E.J. et al. Myrionema strangulans (Chordariales, Phaeophyceae) epiphyte on Ulva spp. (Ulvophyceae) from Patagonian Atlantic coasts. J Appl Phycol 24, 475–486 (2012). https://doi.org/10.1007/s10811-012-9798-0

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